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• We analyzed the population diversity and selection signatures of the high altitude sheep breed Changthangi. • Changthangi was compared to three breed groups, namely European commercial, Indian, and breeds inhabiting plains. • Results revealed multiple functional regions on chromosomes 2, 3, 6 and 18 to be under selection in Changthangi. • The UCP gene family, associated with adaptation to cold and hypoxic conditions, was found to be under selection in Changthangi. Changthangi is a high-altitude sheep breed of India that is adapted to cold and hypoxic climate of Himalayas. In the present study, we analysed population structure of Changthangi and contrasted it with selected Indian and European commercial sheep breeds to detect genomic regions under positive selection. The Illumina OvineSNP50v1 genotype data on 292 animals from seven different sheep breeds i.e., Changthangi (n = 29), Garole (n = 26), Deccani (n = 24), Tibetan (n = 37), Rambouillet (n = 102) and Australian Merino (n = 50) was used. European Mouflon (n = 24) was used as an out-group for studying the stratification and phylogenetic lineage. While the principal component analysis (PCA) revealed Changthangi to cluster with Tibetan sheep; TREEMIX and ADMIXTURE results also detected the introgression of lowland Indian sheep inheritance in Changthangi. Changthangi sheep were compared with other breed groups as reference i.e., commercial (Australian Merino and Rambouillet), Indian (Deccani, Garole and Tibetan) and breeds inhabiting plains (Australian Merino, Rambouillet, Deccani and Garole). Genomic comparisons of Changthangi using cross population extended haplotype homozygosity (XP-EHH) showed multiple functional regions present on Ovis aries (Oar) chromosomes 2, 3, 6 and 18 to be under selection in Changthangi sheep. These regions were related with adaptation to climatic and hypoxic stressors, fleece characteristics and functioning of immune and reproductive systems. UCP genes, associated with adaptation to cold and hypoxic conditions, were the main loci under positive selection in Changthangi sheep population. The selection signals in Indian and European commercial sheep breeds were mainly associated with body weight and carcass traits. Furthermore, selection signals found in different comparisons were found to be part of different quantitative trait loci (QTLs) associated with important traits in different breed classes. The genes present in these regions are suitable candidates for future studies on the genetic mechanisms underlying high-altitude adaptation. [ABSTRACT FROM AUTHOR]